Herbicide resistance and supersensitivity in photosystem II

Abstract. Resistance to triazine herbicides in higher plants was first observed in 1970. A mutation in the photosystem II reaction center D1 protein at position Ser264→Gly is responsible for this resistance. So far, 37 single mutants, 16 double mutants, 5 triple mutants and 5 deletion/insertion mutants in the D1 protein have been obtained by randomly induced and site-directed mutagenesis in cyanobacteria and algae. The influence of these mutations on the binding affinities of different classes of herbicides will be discussed. Because a sufficiently high resolution X-ray structure of photosystem II does not yet exist, the reaction center of purple photosynthetic bacteria, which is homologeous to photosystem II, served as a model. In the bacterial reaction center a total of 25 single and 3 double herbicide-resistant mutants have been generated.

[1]  Hans J. Bohnert,et al.  Nucleotide sequence of the gene for the Mr 32,000 thylakoid membrane protein from Spinacia oleracea and Nicotiana debneyi predicts a totally conserved primary translation product of Mr 38,950 , 1982 .

[2]  G. Ryan.  Resistance of Common Groundsel to Simazine and Atrazine , 1970, Weed Science.

[3]  A. Trebst.  The Topology of the Plastoquinone and Herbicide Binding Peptides of Photosystem II in the Thylakoid Membrane , 1986 .

[4]  G. Stephenson,et al.  Comparative Triazine Effects Upon System II Photochemistry in Chloroplasts of Two Common Lambsquarters (Chenopodium album) Biotypes , 1978, Weed Science.

[5]  L. Mets,et al.  Atrazine, bromacil, and diuron resistance in chlamydomonas: a single non-mendelian genetic locus controls the structure of the thylakoid binding site. , 1984, Plant physiology.

[6]  J. Holtum,et al.  INCREASED DETOXIFICATION IS A MECHANISM OF SIMAZINE RESISTANCE IN LOLIUM-RIGIDUM , 1993 .

[7]  K. Steinback,et al.  Characterization of chloroplast thylakoid polypeptides in the 32-kDa region: polypeptide extraction and protein phosphorylation affect binding of photosystem II-directed herbicides. , 1984, Archives of Biochemistry and Biophysics.

[8]  W. Vermaas,et al.  Synthetic quinones influencing herbicide binding and Photosystem II electron transport. The effects of triazine-resistance on quinone binding properties in thylakoid membranes , 1983 .

[9]  D. Kirilovsky,et al.  S1 Destabilization and Higher Sensitivity to Light in Metribuzin-Resistant Mutants , 1994, Plant physiology.

[10]  M. Edelman,et al.  The D-E region of the D1 protein is involved in multiple quinone and herbicide interactions in photosystem II. , 1994, Biochemistry.

[11]  G. Wildner,et al.  Isolation and characterisation of metribuzin-resistant Chlamydomonas reinhardii cells , 1982 .

[12]  J. Hirschberg,et al.  Triazine Resistance in Phalaris paradoxa: Physiological and Molecular Analyses , 1987 .

[13]  U. Johanningmeier,et al.  Site-specific mutagenesis of the D1 subunit of photosystem II in wild-type Chlamydomonas. , 1991, The Plant cell.

[14]  G. Gardner.  Azidoatrazine: photoaffinity label for the site of triazine herbicide action in chloroplasts. , 1981, Science.

[15]  W. Oettmeier,et al.  Herbicide binding at photosystem II. A new azido-triazinone photoaffinity label , 1984 .

[16]  Yasuyuki Yamada,et al.  A binding model for phenylurea herbicides based on analysis of a Thr264 mutation in the D-1 protein of tobacco , 1989 .

[17]  Mapping of the triazine binding site to a highly conserved region of the QB-protein. , 1986, Archives of biochemistry and biophysics.

[18]  J. Hirschberg,et al.  Molecular Basis of Herbicide Resistance in Amaranthus hybridus , 1983, Science.

[19]  D. Kirilovsky,et al.  Induced New Mutation of D1 Serine-268 in Soybean Photosynthetic Cell Cultures Produced Atrazine Resistance, Increased Stability of S2QB - and S3QB - States, and Increased Sensitivity to Light Stress , 1996, Plant physiology.

[20]  M. Schiffer,et al.  Structure of Rhodopseudomonas sphaeroides R‐26 reaction center , 1986, FEBS letters.

[21]  D C Rees,et al.  Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer. , 1997, Science.

[22]  W. Vermaas.  Molecular-biological approaches to analyze photosystem II structure and function , 1993 .

[23]  Christopher Preston,et al.  Herbicide resistance: Impact and management , 1996 .

[24]  W. Oettmeier,et al.  A single mutation in the M‐subunit of Rhodospirillum rubrum confers herbicide resistance , 1997, FEBS letters.

[25]  D. Grizeau,et al.  Characterization of diuron-resistant Euglena: Greater tolerance for various phenylurea herbicides and increased sensitivity of thylakoids to ethyl-S-dipropyl thiocarbamate , 1983 .

[26]  Govindjee,et al.  Modification of the photosystem II acceptor side function in a D1 mutant (arginine-269-glycine) of Chlamydomonas reinhardti. , 1997, Biochimica et biophysica acta.

[27]  J. Gray,et al.  The molecular basis of triazine herbicide resistance in Senecio vulguris L. , 1986 .

[28]  H. Meyer,et al.  Mapping of two tyrosine residues involved in the quinone‐ (QB) binding site of the D‐1 reaction center polypeptide of photosystem II , 1988 .

[29]  H. Neu,et al.  The Crisis in Antibiotic Resistance , 1992, Science.

[30]  W. Vermaas,et al.  Interactions of herbicides and azidoquinones at a Photosystem II binding site in the thylakoid membrane , 1983 .

[31]  P. Sebban,et al.  Study of wild type and genetically modified reaction centers from Rhodobacter capsulatus: structural comparison with Rhodopseudomonas viridis and Rhodobacter sphaeroides. , 1993, Biophysical journal.

[32]  J. Hearst,et al.  Nucleotide and deduced polypeptide sequences of the photosynthetic reaction-center, B870 antenna, and flanking polypeptides from R. capsulata , 1984, Cell.

[33]  J. Erickson,et al.  Herbicide resistance in Chlamydomonas reinhardtii results from a mutation in the chloroplast gene for the 32-kilodalton protein of photosystem II. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M. Edelman,et al.  Chloroplast-coded atrazine resistance in Solanum nigrum: psbA loci from susceptible and resistant biotypes are isogenic except for a single codon change. , 1984, Nucleic acids research.

[35]  D. Youvan,et al.  A Genetic System for Rapidly Assessing Herbicides That Compete for the Quinone Binding Site of Photosynthetic Reaction Centers , 1989, Bio/Technology.

[36]  C. Vernotte,et al.  A New Ioxynil-Resistant Mutant in Synechocystis PCC 6714: Hypothesis on the Interaction of Ioxynil with the D1 Protein , 1990, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[37]  S. Radosevich,et al.  Modification of Herbicide Binding to Photosystem II in Two Biotypes of Senecio vulgaris L. , 1979, Plant physiology.

[38]  W. Oettmeier,et al.  Metribuzin-Resistant Mutants of Chlamydomonas reinhardii , 1984 .

[39]  D. Youvan,et al.  Genetic Engineering of Herbicide Resistance: Saturation Mutagenesis of Isoleucine 229 of the Reaction Center L Subunit , 1987 .

[40]  D. Ort,et al.  Comparison of Photosynthetic Performance in Triazine-Resistant and Susceptible Biotypes of Amaranthus hybridus. , 1983, Plant physiology.

[41]  K. Tietjen,et al.  The herbicide binding niche of photosystem II‐a model , 1991 .

[42]  C. Jansson,et al.  Mutation: Site-Directed Mutagenesis for Structure-Function Analyses of the Photosystem II Reaction Center Protein D1 , 1997 .

[43]  A. Horovitz,et al.  Predicted effects on herbicide binding of amino acid substitutions in the D1 protein of photosystem II , 1989 .

[44]  J. Deisenhofer,et al.  Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3Å resolution , 1985, Nature.

[45]  C. Vernotte,et al.  Mutation in phenol‐type herbicide resistance maps within the psbA gene in Synechocystis 6714 , 1989, FEBS letters.

[46]  K. Andrews,et al.  Catalytic Sites for Reduction and Oxidation of Quinones , 1987 .

[47]  A. Trebst.  A Contact Site between the Two Reaction Center Polypeptides of Photosystem II Is Involved in Photoinhibition , 1991 .

[48]  S. C. Falco,et al.  The Development of Herbicide Resistant Crops , 1989 .

[49]  James Barber,et al.  Three-dimensional structure of the plant photosystem II reaction centre at 8 Å resolution , 1998, Nature.

[50]  A. Trebst.  The Three-Dimensional Structure of the Herbicide Binding Niche on the Reaction Center Polypeptides of Photosystem II , 1987 .

[51]  R. Haselkorn,et al.  Mutation to herbicide resistance maps within the psbA gene of Anacystis nidulans R2. , 1985, Science.

[52]  J. W. Gronwald,et al.  Atrazine Resistance in a Velvetleaf (Abutilon theophrasti) Biotype Due to Enhanced Glutathione S-Transferase Activity. , 1991, Plant physiology.

[53]  C. Arntzen,et al.  The Mode of Action of Photosystem II-Specific Inhibitors in Herbicide-Resistant Weed Biotypes , 1979 .

[54]  W. Oettmeier,et al.  Effect of different photosystem II inhibitors on chloroplasts isolated from species either susceptible or resistant toward s-triazine herbicides , 1982 .

[55]  Govindjee,et al.  Differential sensitivity of bicarbonate‐reversible formate effects on herbicide‐resistant mutants of Synechocystis 6714 , 1990, FEBS letters.

[56]  W. Kühlbrandt,et al.  Two-dimensional structure of plant photosystem II at 8-Å resolution , 1997, Nature.

[57]  A. Trebst,et al.  Response in the inhibitor efficiency of substituted phenols on ps II activity in six mutants of the D1 protein subunit in Chlamydomonas reinhardtii , 1993 .

[58]  J. Deisenhofer,et al.  Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II , 1988 .

[59]  J. Holtum,et al.  Mechanisms and Agronomic Aspects of Herbicide Resistance , 1993 .

[60]  D. Stalker,et al.  Purification and properties of a nitrilase specific for the herbicide bromoxynil and corresponding nucleotide sequence analysis of the bxn gene. , 1988, The Journal of biological chemistry.

[61]  I. Sinning.  Herbicide binding in the bacterial photosynthetic reaction center. , 1992, Trends in biochemical sciences.

[62]  K. Steinback,et al.  Identification of the triazine receptor protein as a chloroplast gene product. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[63]  I. Ohad,et al.  ASSIGNMENT OF FUNCTION TO POLYPEPTIDES OF 32–34 KILODALTONS IN THYLAKOIDS , 1983 .

[64]  A. Crofts,et al.  Molecular Modelling Studies on the Binding of Phenylurea Inhibitors to the D 1 Protein of Photosystem II , 1990, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[65]  K. Satoh,et al.  Polypeptide composition of a photosystem II core complex: Presence of a herbicide-binding protein. , 1983 .

[66]  J. Deisenhofer,et al.  Pigment—protein interactions in the photosynthetic reaction centre from Rhodopseudomonas viridis , 1986, The EMBO journal.

[67]  G. Friso,et al.  Reduced turnover of the D1 polypeptide and photoactivation of electron transfer in novel herbicide resistant mutants of Synechocystis sp. PCC 6803. , 1997, European journal of biochemistry.

[68]  Determination of the Rate Limiting Step for Photosynthesis in a Nearly Isonuclear Rapeseed (Brassica napus L.) Biotype Resistant to Atrazine. , 1988, Plant physiology.

[69]  J. Gasquez,et al.  Atrazine Resistance in Chenopodium album: Low and High Levels of Resistance to the Herbicide Are Related to the Same Chloroplast PSBA Gene Mutation. , 1987, Plant physiology.

[70]  J. Erickson,et al.  Function and assembly of photosystem II: genetic and molecular analysis. , 1988, Trends in biochemical sciences.

[71]  F. Nagy,et al.  Sequence of the psbA gene from wild type and triazin-resistant Nicotiana plumbaginifolia. , 1988, Nucleic acids research.

[72]  W. Oettmeier,et al.  Structure-activity relationships of triazinone herbicides on resistant weeds and resistant Chlamydomonas reinhardtii , 1991 .

[73]  J. Barber,et al.  Photosystem II. , 1999, Current opinion in structural biology.

[74]  K. Steinback,et al.  Effect of Photosystem II Inhibitors on Thylakoid Membranes of Two Common Groundsel (Senecio vulgaris) Biotypes , 1979, Weed Science.

[75]  K. Steinback,et al.  Photoaffinity labeling of an herbicide receptor protein in chloroplast membranes. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[76]  R. Calvayrac,et al.  Partial Molecular Analysis of the psbA Gene in Euglena gracilis Mutants Exhibiting Resistance to DCMU and Atrazine , 1996, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[77]  J. Erickson,et al.  Herbicide Resistance and Cross-Resistance: Changes at Three Distinct Sites in the Herbicide-Binding Protein , 1985, Science.

[78]  P. Heifetz,et al.  Herbicide Resistance and Growth of D1 Ala251 Mutants in Chlamydomonas , 1997 .

[79]  J. Mullet,et al.  Identification of a 32-34-kilodalton polypeptide as a herbicide receptor protein in photosystem II. , 1981, Biochimica et biophysica acta.

[80]  The mechanism of herbicide resistance in tobacco cells with a new mutation in the q(b) protein. , 1989, Plant physiology.

[81]  Shankar Subramaniam,et al.  Modeling of the D1/D2 proteins and cofactors of the photosystem II reaction center: Implications for herbicide and bicarbonate binding , 1996, Protein science : a publication of the Protein Society.

[82]  D. Stalker,et al.  Herbicide resistance in transgenic plants expressing a bacterial detoxification gene. , 1988, Science.

[83]  N. Ohad,et al.  Mutations resistant to photosystem II herbicides , 1987 .

[84]  U. Johanningmeier,et al.  A new mutation in the gene coding for the herbicide‐binding protein in Chlamydomonas , 1987 .

[85]  J. Höhfeld,et al.  [125I]Azido-Ioxynil Labels Val249 of the Photosystem II D -1 Reaction Center Protein , 1989, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[86]  U. Johanningmeier,et al.  Metribuzin resistance in photoautotrophic Chenopodium rubrum cell cultures , 1993, FEBS letters.

[87]  T. Tomo,et al.  The distance between P680 and QA in Photosystem II determined by ESEEM spectroscopy , 1997 .

[88]  P. Goldsbrough,et al.  A Serine-to-Threonine Substitution in the Triazine Herbicide-Binding Protein in Potato Cells Results in Atrazine Resistance without Impairing Productivity , 1993, Plant physiology.

[89]  W. Draber,et al.  Herbicides in Photosynthesis Research , 1992 .